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Chronic Diseases and Translational Medicine 6 (2020) 79e86
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Review
Pulmonary rehabilitation for patients with coronavirus disease 2019
(COVID-19)
Lu-Lu Yang a,b, Ting Yang b,*
a
Capital Medical University, Beijing 100069, China
b
Department of Pulmonary and Critical Care Medicine, Center of Respiratory Medicine, China-Japan Friendship Hospital, Beijing 100029,
China

Received 27 March 2020


Available online 14 May 2020

Abstract

As a highly infectious respiratory tract disease, coronavirus disease 2019 (COVID-19) can cause respiratory, physical, and
psychological dysfunction in patients. Therefore, pulmonary rehabilitation is crucial for both admitted and discharged patients of
COVID-19. In this study, based on the newly released pulmonary rehabilitation guidelines for patients with COVID-19, as well as
evidence from the pulmonary rehabilitation of patients with severe acute respiratory syndrome, we investigated pulmonary
rehabilitation for patients with COVID-19 having complications, such as chronic pulmonary disease, and established an intelligent
respiratory rehabilitation model for these patients.
© 2020 Chinese Medical Association. Production and hosting by Elsevier B.V. on behalf of KeAi Communications Co., Ltd. This is
an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Keywords: Coronavirus disease 2019 (COVID-19); Pulmonary rehabilitation; Intelligence

Coronavirus Disease 2019 (COVID-19) has spread Prevention and Control of Infectious Diseases,
worldwide and has become a global public health COVID-19 has been classified as a Category B infec-
emergency. The World Health Organization recently tious disease, with prevention and control measures for
declared the outbreak a pandemic. In accordance with Category A infectious diseases adopted against the
the Law of the People's Republic of China on the disease. Multiple COVID-19 diagnosis and treatment
guidelines have been released by the National Health
Commission of the People's Republic of China, all of
which have contributed to the gradual control of the
* Corresponding author. Department of Pulmonary and Critical
Care Medicine, Center of Respiratory Medicine, China-Japan
epidemic. According to the data released by the Na-
Friendship Hospital, No 2, East Yinghua Road, Chaoyang District, tional Health Commission, although more than 84,000
Beijing 100029, China. patients have been diagnosed with COVID-19, over
E-mail address: zryyyangting@163.com (T. Yang). 78,000 patients have now recovered and have been
Peer review under responsibility of Chinese Medical Association. discharged. Since patients with COVID-19 suffer from
various degrees of respiratory, physical, and psycho-
logical dysfunction, pulmonary rehabilitation is
Production and Hosting by Elsevier on behalf of KeAi
equally important for both admitted and discharged

https://doi.org/10.1016/j.cdtm.2020.05.002
2095-882X/© 2020 Chinese Medical Association. Production and hosting by Elsevier B.V. on behalf of KeAi Communications Co., Ltd. This is an
open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
80 L.-L. Yang, T. Yang / Chronic Diseases and Translational Medicine 6 (2020) 79e86

patients for the treatment of the disease.1 For this and arbidol. According to the summary of phased
reason, several pulmonary rehabilitation guidelines for treatment of patients with COVID-19 in China, the
patients with COVID-19 have been published in China clinical efficacy of lopinavir/ritonavir for antiviral
to strengthen the pulmonary rehabilitation of admitted treatment is not obvious, and Lopinavir/Ritonavir is
patients and follow-up and health management of associated with several side effects; hence, the drug is
discharged patients and thereby help the patients to not recommended for use at present.10 The indirect
recover and return to society more promptly and safely. evidence for efficacy of Ribavirin and IFN in the
treatment of COVID-19 has been mainly derived from
Pulmonary rehabilitation the evidence of the efficacy of the drugs in treatment of
infections caused by severe acute respiratory syndrome
Pulmonary rehabilitation refers to the individualized (SARS) and middle east respiratory syndrome
rehabilitation treatment of patients with chronic pul- (MERS).11,12 However, patients with COVID-19
monary diseases after a detailed assessment. With ex- treated with IFN-a 2b in combination with Ribavirin
ercise training as its core, pulmonary rehabilitation have no significant improvement in the risk of death
comprises comprehensive interventions, including but compared to those treated with IFN-a 2b alone.13 The
not limited to psychological and nutritional support, as latest research shows that chloroquine can effectively
well as education and behavioral changes.2 The goal of inhibit severe acute respiratory syndrome coronavirus
pulmonary rehabilitation is to not only improve the 2 (SARS-CoV-2) infection at the cellular level.14
patient's physical and mental conditions but also help Furthermore for patients with a history of local
the patient return to family and society more promptly. epidemiology or other risk factors related to infection
With the development of evidence-based medicine, (including travel history or exposure to animal influ-
progressively more information has been obtained, enza virus), oseltamivir can be empirically added to the
based on which it is recommended that pulmonary treatment regimen.15 Some scholars also think that
rehabilitation should be the core of standardized remdesivir, darunavir/cobicistat, and favipiravir could
management of patients with chronic obstructive pul- be used in the treatment of COVID-19. At present, a
monary disease (COPD) and a treatment option for number of randomized controlled trials are in progress
patients with other chronic pulmonary diseases. The to evaluate the efficacy and safety of the above-
“Global Initiative for Obstructive Lung Disease mentioned drugs for the treatment of COVID-19.
(GOLD)” incorporated pulmonary rehabilitation into The three major components of the medical sys-
the standard treatment for patients with COPD as early temdprevention, treatment, and rehabilitationdare
as 2001.3 The “Healthy China Initiative (2019e2030)” equally important. The primary clinical manifestations
issued in 2019 has also emphasized the necessity of of COVID-19 are fever, cough, dyspnea, and
including pulmonary rehabilitation in a chronic pul- myalgia16; however, severe cases can rapidly progress
monary disease action plan.4 Furthermore, several to acute respiratory distress syndrome (ARDS). In
high-quality clinical studies have verified the benefits addition, some patients can develop acute myocardial
of pulmonary rehabilitation for inpatients, outpatients, and kidney injuries.17 The latest pathological reports
and inehome patients. The benefits include improved indicate that the predominant pathological changes in
exercise tolerance in patients with chronic pulmonary early-18 and late-stage patients are diffuse lung in-
diseases, reduced number of hospital admissions and juries, although some patients also suffer from intra-
length of hospital stays, enhanced health-related qual- alveolar fibrinous exudate and pulmonary interstitial
ity of life,5 improved respiratory muscle function and fibrosis. Moreover, the virus also affects other organs
relieved dyspnea,6 alleviated disease-related anxiety such as the heart, liver, and kidneys to various de-
and depression,7 and enhanced skeletal muscle func- grees.19 These changes contribute to hypoxemia and
tion of upper and lower limbs.8,9 impaired cardiopulmonary and organ functions
throughout the body. Currently, evidence on the prog-
Necessity of pulmonary rehabilitation for patients nosis of patients with COVID-19 is insufficient, espe-
with COVID-19 cially for elderly patients in whom the disease is
complicated by other basic diseases. It remains unclear
At present, the main antiviral drugs that are rec- whether the impairment of multiple systemic functions
ommended for the treatment of COVID-19 are inter- is reversible or if the long-term existence of the virus
feron-a (IFN-a), lopinavir/ritonavir, ribavirin, can cause physical dysfunction in these patients. In
chloroquine phosphate, hydroxychloroquine sulfate, addition, because COVID-19 has caused a public
L.-L. Yang, T. Yang / Chronic Diseases and Translational Medicine 6 (2020) 79e86 81

emergency, patients with COVID-19 may demonstrate relevant health education. Compared with patients in
different degrees of psychological disorders, such as the control group who only received conventional care,
anger, fear, anxiety, depression, insomnia, and loneli- patients in the rehabilitation group showed significant
ness, as well as a lack of cooperation and abandonment differences in 6-minute walking distance and
of treatment due to fear of the disease.20 Even when maximum rate of oxygen consumption during incre-
discharged, the patients may experience post-traumatic mental exercise. In addition, the isometric muscle
stress syndrome. Therefore, prompt introduction and strength of the anterior deltoid muscle and gluteus
continuous availability of pulmonary rehabilitation maximus, the grip strength of both hands (distal muscle
services is critical for patients with COVID-19. strength), and results of the 1-minute curl and push-up
test (endurance of abdominal and upper limb muscles)
Evidence for pulmonary rehabilitation of patients were all substantially elevated in the rehabilitation
with SARS group. However, although the role-physical, role-
emotional, and social function scales of the SF-36
Follow-up studies have shown that after discharge, questionnaire had improved within 6 weeks in the
patients with severe acute respiratory syndrome rehabilitation group, the pairwise differences were
(SARS) can still suffer from symptoms, such as insignificant, possibly due to the extensive physical
restrictive pulmonary dysfunction, palpitations, hand and psychological impacts of SARS on the patients
tremors, and exertional dyspnea, all of which affect (especially elderly patients). Furthermore, patients who
their daily activities and impair their quality of life.21,22 were not reinstated (predominantly healthcare workers)
It has been suggested that these symptoms are associ- scored lower on almost all scales (except bodily pain)
ated with prolonged bed rest, adverse effects of steroid than patients who were reinstated prior to the
medications, and residual pathological changes, such completion of the intervention, indicating that prompt
as atelectasis, persistent alveolitis, pulmonary fibrosis, reinstatement can help improve the patients’ quality of
and varying degrees of muscle weakness or dysfunc- life. Alternatively, a small sample study in China on 9
tion.23 In addition, a 1-year follow-up of patients with discharged patients with SARS who underwent 3
ARDS showed that, survivors of ARDS exhibit weeks of rehabilitation consisting of respiratory exer-
persistent functional disability one year after discharge cises combined with deep breathing and stretching
from the intensive care unit. Most patients have exercises, low-to medium-intensity treadmill aerobic
extrapulmonary conditions, with muscle wasting and endurance exercise, and direct-current iontophoresis
weakness being most prominent.24 Compared with pulmonary physiotherapy, suggested that the perfusion
SARS, pathological changes, such as pulmonary rate for pulmonary function of the patients was
fibrosis, have not been dominant in patients with significantly different from the baseline value. In
COVID-19; however, we speculate that damage to the addition, the dyspnea level of the rehabilitation group
lung and other organ systems caused by SARS-CoV-2, improved considerably compared to that of the control
especially in severe patients with ARDS, may lead to group, while the resting heart rates of both groups
residual physical dysfunction of varying degrees. Thus, recovered to a certain extent.26
the evidence for pulmonary rehabilitation of patients
with SARS provides strong support and reference for Pulmonary rehabilitation guidelines for patients
the development of pulmonary rehabilitation programs with COVID-19
for patients with COVID-19.
Lau et al25 carried out a 6-week pulmonary reha- Based on front-line expert consensus and refer-
bilitation program for 133 patients with SARS who had ences, rehabilitation specialists in China have devel-
been discharged after treatment. Each rehabilitation oped practical and feasible respiratory rehabilitation
session was conducted for 1.0e1.5 h, 4e5 times per guidelines for patients with COVID-19. The primary
week. The interventions included 30e40 min of aero- instructions of these guidelines are as follows: (1) The
bic training at 60%e75% (up to 80%e85% for some short-term goal of pulmonary rehabilitation is to alle-
subjects) of maximum heart rate predicted using the viate dyspnea and relieve anxiety and depression while
Chester Step Test to reach a score of 4e6 on the Borg the long-term goal is to preserve the patient's function
Rating of Perceived Exertion, followed by 3 sets of to the maximum extent, improve his/her quality of life,
upper and lower limb resistance exercises at 10e15 and facilitate his/her return to society. (2) It is neces-
RM (repetition maximum, the maximum load that can sary to perform comprehensive assessments before
be repeated with 10e15 movements in each set) and starting the rehabilitation program. For example,
82 L.-L. Yang, T. Yang / Chronic Diseases and Translational Medicine 6 (2020) 79e86

clinical and exercise risk assessments should be per- resources, movement of severely or critically ill pa-
formed based on the patient's clinical symptoms, vital tients should be limited to their bed or bedside. Once
signs, auxiliary examinations, imaging, comorbidities, discharged, patients should continue individualized
contraindications, etc., whereas quality of life, daily rehabilitation under the premise of strengthening pro-
activity endurance, and psychological and nutritional tection and prevention against other infectious diseases
assessments should be conducted in the form of such as cold. (5) Compared with general rehabilitation
questionnaires. The results of these assessments can for patients with chronic diseases, the most distinctive
then be combined with the patient's aerobic endurance, characteristic of rehabilitation for patients with
muscle strength, balance, and flexibility to formulate COVID-19 is the infectivity of the disease. Therefore,
an individualized and progressive rehabilitation pre- operations that can increase the risk of infection, such
scription. The prescription content mostly includes: A. as instructed cough, expiration training, and tracheal
Aerobic exercises: walking, fast walking, jogging, compression, should be minimized. A sealed plastic
swimming, etc., starting from low intensity and grad- bag should be used to cover the mouth during expec-
ually improving the intensity and duration, 3e5 times a toration to prevent infection. In addition, pulmonary
week, 20e30 min each time. B. Strength training: rehabilitation of patients with COVID-19 should be
progressive resistance training is recommended. The carried out mainly through educational videos, bro-
training load of each target muscle group is 8e12 RM, chures, remote consultations, or online teaching so as
1e3 groups/time. The training interval of each group is to save protective equipment and avoid cross infection.
2 minutes, 2e3 times/week, and the training load is (6) Evaluation and monitoring should be conducted
increased by 5%e10% every week. C. Balance throughout the pulmonary rehabilitation program.27,28
training: Patients with balance dysfunction should be An example of the rehabilitation of a patient with
involved in balance training, including unarmed bal- COVID-19 is provided below.
ance training and balance training instrument. D. Patient A is a male, 50 years old, and critically ill
Respiratory training: if the patient has symptoms, such with COVID-19. Prior to rehabilitation, the patient was
as shortness of breath, wheezing, and difficulty in treated in the ICU for 1 month before he underwent
expectoration after discharge, respiratory mode hormone therapy for over 1 month. The computer to-
training, such as body position management, adjust- mography (CT) displayed diffuse pulmonary lesions in
ment of respiratory rhythm, traction of respiratory both lungs, as shown in Fig. 1. Table 1 lists the patient's
muscle group breathing exercise, and expectoration assessment results prior to rehabilitation, and Table 2
training, should be arranged in combination with the lists the patient's individualized rehabilitation pre-
evaluation results. E. Health care training for using scription based on the assessment.
traditional Chinese medicine: it is mainly for light and
ordinary patients and discharged patients. If there is no Thoughts on pulmonary rehabilitation of patients
contraindication (such as limb dysfunction and with COVID-19 complicated with chronic pulmo-
abnormal consciousness), it is recommended to carry nary diseases
out Baduan jin, Twenty-four Simplified Tai chi, Six-
word Qigong, etc., 30e50 min each time, once a day. For patients with COVID-19 complicated with
(3) All rehabilitation should be carried out under the chronic pulmonary diseases, such as COPD, bronchial
premise of safety. In case a patient shows peripheral asthma, and pulmonary interstitial fibrosis, in addition
capillary oxygen saturation (SpO2) < 88% or develops to performing an assessment and developing a pre-
symptoms, such as palpitations, sweating, chest tight- scription based on the rehabilitation guidelines, the
ness, and shortness of breath, which are deemed un- following instructions should be followed: (1) Ensure
suitable for rehabilitation by the clinician, then the the continuation of standardized basic medications and
rehabilitation program should be terminated immedi- a reasonable diet. (2) Promote smoking cessation, flu
ately. (4) For mild and moderate cases, rehabilitation vaccination, and Streptococcus pneumoniae vaccina-
interventions should be introduced as early as possible. tion. (3) As patients with COVID-19 having chronic
In contrast, for severe and critical cases, life-saving pulmonary diseases often have excessive airway se-
measures should be prioritized when the patient's cretions, expiration exercises should be performed in
condition is unstable or the disease is still progressing. addition to general airway clearance exercises to
In such cases, pulmonary rehabilitation interventions facilitate sputum excretion and reduce the exhaustion
should be introduced only when the patient's condition due to coughing. In addition, auxiliary techniques,
has stabilized. In addition, in view of safety and human such as the application of oscillatory positive
L.-L. Yang, T. Yang / Chronic Diseases and Translational Medicine 6 (2020) 79e86 83

Fig. 1. Diffuse pulmonary lesions in both lungs of the COVID-19 patient.

expiratory pressure (OPEP), can be utilized. (4) volume, dead space ventilation and work of breathing,
Appropriate oxygen therapy should be provided during thereby further reducing blood oxygen saturation. In
exercises. Patients with chronic pulmonary diseases contrast, introducing oxygen therapy during exercise
can develop hypoxemia at rest. Subsequently, when can meet the elevated metabolic demands, prevent
exercising, as the interval for red blood cells to pass hypoxemia, and reduce pulmonary dynamic hyperin-
through the alveolar capillaries is shortened, the flation, thereby improving the effect of exercise, while
ventilation flow rate disorder increases, and oxygen allowing an increase in the intensity and duration of the
intake decreases. Meanwhile, an escalated breathing exercise. Hypoxemia during exercise is regarded as the
rate causes pulmonary dynamic hyperinflation and gas indication for requirement of oxygen therapy (SpO2 at
trapping, which increases the end-expiratory lung 88%e90% or a relative reduction of 2%e5%, lasting

Table 1
Assessment results before rehabilitation.
Assessment Items Assessment Result Suggested Issue
Breath-hold test Less than 10 seconds (normally 30 seconds) Impaired lung function
1-minute step test Heart rate before and after the test 102e124 beats/minute Severely declined cardiopulmonary endurance
Blood oxygen change 97%e94%
Borg Dyspnea Scale score 0e2
Squat Cannot complete independently Lower limb muscle atrophy and reduced
muscle function

Table 2
Individualized rehabilitation prescription.
Prescription Items Content Required Equipment
Improve dyspnea Diaphragmatic breathing þ constricted breathing, 10 minutes, 3 Bare hands
times/day
Airway clearance Expiration training þ sputum excretion device, 15 minutes, 1 time/ Sputum excretion and breathing trainer
day
Respiratory muscle exercise Non-threshold load training for the inspiratory muscle, started from Respiratory muscle trainer
3 cm H2O and slowly increased thereafter, 10e15 minutes, 1 time/
day
Thoracic expansion exercise Stretching, 5 minutes, 1 time/day Bare hands
Activity 10e30 minutes, either walking or stepping, target heart rate 124 Heart rate monitor and oximeter
beats/minute, Borg score 2, blood oxygen no less than 90%
Resistance exercise Bare hands, yellow elastic band, big muscle group, 10 minutes/time Elastic band
Nutritional support Protein powder for muscular dystrophy, 1e12 g/kg Protein powder
84 L.-L. Yang, T. Yang / Chronic Diseases and Translational Medicine 6 (2020) 79e86

for 0.5e5.0 min). The goal of oxygen therapy is to directly obtain an individualized rehabilitation pre-
adjust the oxygen flow rate to maintain the SpO2 scription through the application, followed by video
within the range of 90%e92%. In order to increase the training and recordings of rehabilitation exercises. In
exercise effect, the oxygen flow rate can be increased addition, the mobile app is capable of functions, such
according to the exercise intensity to maintain the as symptom assessment and recording, automatic re-
SpO2 at about 95%.29 (5) Thoracic kyphosis correc- minders for medication intake, and health education.
tion: Due to long-term dyspnea, cough, etc., the work All acquired data are transmitted to the management
of breathing in patients with chronic pulmonary dis- terminal of the medical care platform through infor-
eases often increases, which leads to the formation of mation and communication technology, so that the
abnormal breathing patterns. The resultant chronic medical staff can remotely monitor and evaluate the
pulmonary hyperinflation usually causes enlargement information provided by the patient on a regular basis
of the anterior and posterior diameters of the chest, and introduce corresponding measures and in-
thereby resulting in barrel chest or other chest de- terventions. This randomized controlled clinical trial to
formities. A study of 143 young patients with cystic evaluate the benefits of rehabilitation is still ongoing. It
fibrosis showed that in patients over 15 years old, the is expected that this remote model will not only reduce
condition of 77% of females and 36% of males was direct contact and exposure between doctors and pa-
complicated with thoracic kyphosis deformity of more tients, thereby preventing infection and saving pro-
than 40 .30 Since this deformity can inhibit airway tective equipment, but also provide long-term benefits
clearance and increase the work of breathing, it is to patients, such as improvement in cardiopulmonary
important to incorporate physiotherapy, such as chest endurance, recovery of physical function, and reduc-
and muscle stretching and intensive training, in a tion of anxiety and depression, thereby promoting pa-
comprehensive pulmonary rehabilitation program for tients' return to society with an enhanced quality of
thoracic kyphosis correction. life.

Exploration and implementation of intelligent Conclusion and outlook


pulmonary rehabilitation for patients with
COVID-19 The development of rehabilitation medicine has
been promoting the transformation of traditional, pas-
The strong infectivity of COVID-19 and dispersal of sive, and fractured medical care models into a human-
discharged patients make it difficult to realize remote oriented healthcare system that covers all stages of life.
pulmonary rehabilitation. At present, there is insuffi- Pulmonary rehabilitation should be provided
cient research on the clinical implementation of remote throughout the diseases management process, regard-
pulmonary rehabilitation. In recent years, rapid devel- less of whether the patient is hospitalized or at home. In
opment in Internet technology has facilitated the addition, rehabilitation prescriptions should be indi-
implementation of remote monitoring and mobile in- vidualized based on the patient's specific condition. The
telligence technologies. The use of information and effective incorporation of pulmonary rehabilitation into
communication technology together with wearable disease management and a patient's daily life, so that it
devices has made it possible to practice intelligent, becomes a conscious behavior, can provide long-term
digital remote rehabilitation for patients with chronic benefits to both the patient and his/her family. With
pulmonary diseases, the effectiveness and safety of the deepening of the understanding of COVID-19, an
which have been proven non-inferior to those of increasing number of patients have recovered. Pulmo-
traditional approaches.31,32 Based on this, we have nary rehabilitation for these recovered patients has
pioneered the implementation of Internet-assisted become a major challenge for medical staff, the reso-
pulmonary rehabilitation in Wuhan's mobile cabin lution of which requires multidisciplinary collaboration
hospitals. During the process, rehabilitation content is and joint exploration so that evidence-based, high-
imported into a dedicated rehabilitation mobile appli- quality support can be provided. In addition, the
cation in text and video formats, including barehanded implementation of both traditional and research-based
aerobic training, resistance training with elastic band, pulmonary rehabilitation provides valuable experience
and respiratory muscle traction exercise. Once a pa- for clinical and rehabilitation medicine practices, which
tient has downloaded the application, he/she can is necessary to implement the “Healthy China” concept.
L.-L. Yang, T. Yang / Chronic Diseases and Translational Medicine 6 (2020) 79e86 85

Funding coronavirus: a preliminary report of two cases. Antivir Ther.


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Edited by Yi Cui

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